Skip to main content
Top
Published in: Virology Journal 1/2006

Open Access 01-12-2006 | Short report

Induction of neutralising antibodies by virus-like particles harbouring surface proteins from highly pathogenic H5N1 and H7N1 influenza viruses

Authors: Judit Szécsi, Bertrand Boson, Per Johnsson, Pia Dupeyrot-Lacas, Mikhail Matrosovich, Hans-Dieter Klenk, David Klatzmann, Viktor Volchkov, François-Loïc Cosset

Published in: Virology Journal | Issue 1/2006

Login to get access

Summary

There is an urgent need to develop novel approaches to vaccination against the emerging, highly pathogenic avian influenza viruses. Here, we engineered influenza viral-like particles (Flu-VLPs) derived from retroviral core particles that mimic the properties of the viral surface of two highly pathogenic influenza viruses of either H7N1 or H5N1 antigenic subtype. We demonstrate that, upon recovery of viral RNAs from a field strain, one can easily generate expression vectors that encode the HA, NA and M2 surface proteins of either virus and prepare high-titre Flu-VLPs. We characterise these Flu-VLPs incorporating the HA, NA and M2 proteins and we show that they induce high-titre neutralising antibodies in mice.
Appendix
Available only for authorised users
Literature
1.
go back to reference Nicholson KG, Wood JM, Zambon M: Influenza. Lancet 2003, 362: 1733-1745. 10.1016/S0140-6736(03)14854-4CrossRefPubMed Nicholson KG, Wood JM, Zambon M: Influenza. Lancet 2003, 362: 1733-1745. 10.1016/S0140-6736(03)14854-4CrossRefPubMed
2.
go back to reference Webby RJ, Webster RG: Are we ready for pandemic influenza? Science 2003, 302: 1519-1522. 10.1126/science.1090350CrossRefPubMed Webby RJ, Webster RG: Are we ready for pandemic influenza? Science 2003, 302: 1519-1522. 10.1126/science.1090350CrossRefPubMed
3.
go back to reference Francis TJ: Vaccination against influenza. Bull World Health Organ 1953, 8: 725-741.PubMed Francis TJ: Vaccination against influenza. Bull World Health Organ 1953, 8: 725-741.PubMed
4.
go back to reference Hilleman MR: Realities and enigmas of human viral influenza: pathogenesis, epidemiology and control. Vaccine 2002, 20: 3068-3087. 10.1016/S0264-410X(02)00254-2CrossRefPubMed Hilleman MR: Realities and enigmas of human viral influenza: pathogenesis, epidemiology and control. Vaccine 2002, 20: 3068-3087. 10.1016/S0264-410X(02)00254-2CrossRefPubMed
5.
go back to reference Tamura S, Tanimoto T, Kurata T: Mechanisms of broad cross-protection provided by influenza virus infection and their application to vaccines. Jpn J Infect Dis 2005, 58: 195-207.PubMed Tamura S, Tanimoto T, Kurata T: Mechanisms of broad cross-protection provided by influenza virus infection and their application to vaccines. Jpn J Infect Dis 2005, 58: 195-207.PubMed
6.
7.
go back to reference Hoffmann E, Krauss S, Perez D, Webby R, Webster RG: Eight-plasmid system for rapid generation of influenza virus vaccines. Vaccine 2002, 20: 3165-3170. 10.1016/S0264-410X(02)00268-2CrossRefPubMed Hoffmann E, Krauss S, Perez D, Webby R, Webster RG: Eight-plasmid system for rapid generation of influenza virus vaccines. Vaccine 2002, 20: 3165-3170. 10.1016/S0264-410X(02)00268-2CrossRefPubMed
8.
go back to reference Ohuchi M, Cramer A, Vey M, Ohuchi R, Garten W, Klenk HD: Rescue of vector expressed fowl plague virus hemagglutinin in biologically active form by acidotropic agents and coexpressed M2 protein. J Virol 1994, 68: 920-926.PubMedCentralPubMed Ohuchi M, Cramer A, Vey M, Ohuchi R, Garten W, Klenk HD: Rescue of vector expressed fowl plague virus hemagglutinin in biologically active form by acidotropic agents and coexpressed M2 protein. J Virol 1994, 68: 920-926.PubMedCentralPubMed
9.
go back to reference Puthavathana P, Auewarakul P, Charoenying PC, Sangsiriwut K, Pooruk P, Boonnak K, Khanyok R, Thawachsupa P, Kijphati R, Sawanpanyalert P: Molecular characterization of the complete genome of human influenza H5N1 virus isolates from Thailand. J Gen Virol 2005, 86: 423-433. 10.1099/vir.0.80368-0CrossRefPubMed Puthavathana P, Auewarakul P, Charoenying PC, Sangsiriwut K, Pooruk P, Boonnak K, Khanyok R, Thawachsupa P, Kijphati R, Sawanpanyalert P: Molecular characterization of the complete genome of human influenza H5N1 virus isolates from Thailand. J Gen Virol 2005, 86: 423-433. 10.1099/vir.0.80368-0CrossRefPubMed
10.
go back to reference Amonsin A, Payungporn S, Theamboonlers A, Thanawongnuwech R, Suradhat S, Pariyothorn N, Tantilertcharoen R, Damrongwantanapokin S, Buranathai C, Chaisingh A, Songserm T, Poovorawan Y: Genetic characterization of H5N1 influenza A viruses isolated from zoo tigers in Thailand. Virology 2006, 344: 480-491. 10.1016/j.virol.2005.08.032CrossRefPubMed Amonsin A, Payungporn S, Theamboonlers A, Thanawongnuwech R, Suradhat S, Pariyothorn N, Tantilertcharoen R, Damrongwantanapokin S, Buranathai C, Chaisingh A, Songserm T, Poovorawan Y: Genetic characterization of H5N1 influenza A viruses isolated from zoo tigers in Thailand. Virology 2006, 344: 480-491. 10.1016/j.virol.2005.08.032CrossRefPubMed
11.
go back to reference Skehel JJ, Wiley DC: Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu Rev Biochem 2000, 69: 531-569. 10.1146/annurev.biochem.69.1.531CrossRefPubMed Skehel JJ, Wiley DC: Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu Rev Biochem 2000, 69: 531-569. 10.1146/annurev.biochem.69.1.531CrossRefPubMed
12.
go back to reference Bucher D, Palese P: The biologically active proteins of influenza virus: neuraminidase. In The influenza viruses and influenza. Edited by: Kilbourne ED. New York, Academic Press; 1975:83-123. Bucher D, Palese P: The biologically active proteins of influenza virus: neuraminidase. In The influenza viruses and influenza. Edited by: Kilbourne ED. New York, Academic Press; 1975:83-123.
13.
go back to reference Matrosovich MN, Matrosovich TY, Gray T, Roberts NA, Klenk HD: Neuraminidase is important for the initiation of influenza virus infection in human airway epithelium. J Virol 2004, 78: 12665-12667. 10.1128/JVI.78.22.12665-12667.2004PubMedCentralCrossRefPubMed Matrosovich MN, Matrosovich TY, Gray T, Roberts NA, Klenk HD: Neuraminidase is important for the initiation of influenza virus infection in human airway epithelium. J Virol 2004, 78: 12665-12667. 10.1128/JVI.78.22.12665-12667.2004PubMedCentralCrossRefPubMed
14.
go back to reference Lamb RA, Holsinger LJ, Pinto LH: The influenza A virus M2 ion channel protein and its role in the influenza virus life cycle. In Cellular receptors of animal viruses. Edited by: Wimmer E. Cold Spring Harbor, Cold Spring Harbor Laboratory; 1994:303-321. Lamb RA, Holsinger LJ, Pinto LH: The influenza A virus M2 ion channel protein and its role in the influenza virus life cycle. In Cellular receptors of animal viruses. Edited by: Wimmer E. Cold Spring Harbor, Cold Spring Harbor Laboratory; 1994:303-321.
15.
go back to reference Hay AJ: The action of adamantanamines against influenza A viruses: inhibition of the M2 ion channel protein. Semin Virol 1992, 3: 21-30. Hay AJ: The action of adamantanamines against influenza A viruses: inhibition of the M2 ion channel protein. Semin Virol 1992, 3: 21-30.
16.
go back to reference Hatziioannou T, Valsesia-Wittmann S, Russell SJ, Cosset FL: Incorporation of fowl plague virus hemagglutinin into murine leukemia virus particles and analysis of the infectivity of the pseudotyped retroviruses. J Virol 1998, 72: 5313-5317.PubMedCentralPubMed Hatziioannou T, Valsesia-Wittmann S, Russell SJ, Cosset FL: Incorporation of fowl plague virus hemagglutinin into murine leukemia virus particles and analysis of the infectivity of the pseudotyped retroviruses. J Virol 1998, 72: 5313-5317.PubMedCentralPubMed
17.
go back to reference Sandrin V, Boson B, Salmon P, Gay W, Nègre D, LeGrand R, Trono D, Cosset FL: Lentiviral vectors pseudotyped with a modified RD114 envelope glycoprotein show increased stability in sera and augmented transduction of primary lymphocytes and CD34+ cells derived from human and non-human primates. Blood 2002, 100: 823-832. 10.1182/blood-2001-11-0042CrossRefPubMed Sandrin V, Boson B, Salmon P, Gay W, Nègre D, LeGrand R, Trono D, Cosset FL: Lentiviral vectors pseudotyped with a modified RD114 envelope glycoprotein show increased stability in sera and augmented transduction of primary lymphocytes and CD34+ cells derived from human and non-human primates. Blood 2002, 100: 823-832. 10.1182/blood-2001-11-0042CrossRefPubMed
18.
go back to reference Sandrin V, Cosset FL: Intracellular versus cell surface assembly of retroviral pseudotypes is determined by the cellular localization of the viral glycoprotein, its capacity to interact with Gag, and the expression of the Nef protein. J Biol Chem 2006, 281: 528-542. 10.1074/jbc.M506070200CrossRefPubMed Sandrin V, Cosset FL: Intracellular versus cell surface assembly of retroviral pseudotypes is determined by the cellular localization of the viral glycoprotein, its capacity to interact with Gag, and the expression of the Nef protein. J Biol Chem 2006, 281: 528-542. 10.1074/jbc.M506070200CrossRefPubMed
19.
go back to reference Szecsi J, Drury R, Josserand V, Grange MP, Boson B, Hartl I, Schneider R, Buchholz C, Coll JL, Russell SJ, Cosset FL, Verhoeyen E: Targeted retroviral vectors displaying a cleavage site-engineered hemagglutinin (HA) through HA-protease interactions. Mol Ther 2006., in press: Szecsi J, Drury R, Josserand V, Grange MP, Boson B, Hartl I, Schneider R, Buchholz C, Coll JL, Russell SJ, Cosset FL, Verhoeyen E: Targeted retroviral vectors displaying a cleavage site-engineered hemagglutinin (HA) through HA-protease interactions. Mol Ther 2006., in press:
20.
go back to reference Bellier B, Dalba C, Clerc B, Desjardins D, Drury R, Cosset FL, Collins M, Klatzmann D: DNA vaccines encoding retrovirus-based virus-like particles induce efficient immune responses without adjuvant. Vaccine 2006, 24: 2643-2655. 10.1016/j.vaccine.2005.11.034CrossRefPubMed Bellier B, Dalba C, Clerc B, Desjardins D, Drury R, Cosset FL, Collins M, Klatzmann D: DNA vaccines encoding retrovirus-based virus-like particles induce efficient immune responses without adjuvant. Vaccine 2006, 24: 2643-2655. 10.1016/j.vaccine.2005.11.034CrossRefPubMed
21.
go back to reference Bartosch B, Vitelli A, Granier C, Goujon C, Dubuisson J, Pascale S, Scarselli E, Cortese R, Nicosia A, Cosset FL: Cell entry of hepatitis C virus requires a set of co-receptors that include the CD81 tetraspanin and the SR-B1 scavenger receptor. J Biol Chem 2003, 278: 41624-41630. 10.1074/jbc.M305289200CrossRefPubMed Bartosch B, Vitelli A, Granier C, Goujon C, Dubuisson J, Pascale S, Scarselli E, Cortese R, Nicosia A, Cosset FL: Cell entry of hepatitis C virus requires a set of co-receptors that include the CD81 tetraspanin and the SR-B1 scavenger receptor. J Biol Chem 2003, 278: 41624-41630. 10.1074/jbc.M305289200CrossRefPubMed
22.
go back to reference Negre D, Mangeot PE, Duisit G, Blanchard S, Vidalain PO, Leissner P, Winter AJ, Rabourdin-Combe C, Mehtali M, Moullier P, Darlix JL, Cosset FL: Characterization of novel safe lentiviral vectors derived from simian immunodeficiency virus (SIVmac251) that efficiently transduce mature human dendritic cells. Gene Ther 2000, 7: 1613-1623. 10.1038/sj.gt.3301292CrossRefPubMed Negre D, Mangeot PE, Duisit G, Blanchard S, Vidalain PO, Leissner P, Winter AJ, Rabourdin-Combe C, Mehtali M, Moullier P, Darlix JL, Cosset FL: Characterization of novel safe lentiviral vectors derived from simian immunodeficiency virus (SIVmac251) that efficiently transduce mature human dendritic cells. Gene Ther 2000, 7: 1613-1623. 10.1038/sj.gt.3301292CrossRefPubMed
23.
go back to reference Bartosch B, Dubuisson J, Cosset FL: Infectious hepatitis C virus pseudo-particles containing functional E1-E2 envelope protein complexes. J Exp Med 2003, 197: 633-642. 10.1084/jem.20021756PubMedCentralCrossRefPubMed Bartosch B, Dubuisson J, Cosset FL: Infectious hepatitis C virus pseudo-particles containing functional E1-E2 envelope protein complexes. J Exp Med 2003, 197: 633-642. 10.1084/jem.20021756PubMedCentralCrossRefPubMed
24.
go back to reference Bartosch B, Bukh J, Meunier JC, Granier C, Engle RE, Blackwelder WC, Emerson SU, Cosset FL, Purcell RH: In vitro assay for neutralizing antibody to hepatitis C virus: evidence for broadly conserved neutralization epitopes. Proc Natl Acad Sci U S A 2003, 100: 14199-14204. 10.1073/pnas.2335981100PubMedCentralCrossRefPubMed Bartosch B, Bukh J, Meunier JC, Granier C, Engle RE, Blackwelder WC, Emerson SU, Cosset FL, Purcell RH: In vitro assay for neutralizing antibody to hepatitis C virus: evidence for broadly conserved neutralization epitopes. Proc Natl Acad Sci U S A 2003, 100: 14199-14204. 10.1073/pnas.2335981100PubMedCentralCrossRefPubMed
25.
go back to reference Lavillette D, Morice Y, Germanidis G, Donot P, Soulier A, Pagkalos E, Sakellariou G, Intrator L, Bartosch B, Pawlotsky JM, Cosset FL: Human serum facilitates hepatitis C virus infection, and neutralizing responses inversely correlate with viral replication kinetics at the acute phase of hepatitis C virus infection. J Virol 2005, 79: 6023-6034. 10.1128/JVI.79.10.6023-6034.2005PubMedCentralCrossRefPubMed Lavillette D, Morice Y, Germanidis G, Donot P, Soulier A, Pagkalos E, Sakellariou G, Intrator L, Bartosch B, Pawlotsky JM, Cosset FL: Human serum facilitates hepatitis C virus infection, and neutralizing responses inversely correlate with viral replication kinetics at the acute phase of hepatitis C virus infection. J Virol 2005, 79: 6023-6034. 10.1128/JVI.79.10.6023-6034.2005PubMedCentralCrossRefPubMed
26.
go back to reference Bosch V, Kramer B, Pfeiffer T, Starck L, Steinhauer DA: Inhibition of release of lentivirus particles with incorporated human influenza virus haemagglutinin by binding to sialic acid-containing cellular receptors. J Gen Virol 2001, 82: 2485-2494.CrossRefPubMed Bosch V, Kramer B, Pfeiffer T, Starck L, Steinhauer DA: Inhibition of release of lentivirus particles with incorporated human influenza virus haemagglutinin by binding to sialic acid-containing cellular receptors. J Gen Virol 2001, 82: 2485-2494.CrossRefPubMed
27.
go back to reference McKay T, Patel M, Pickles RJ, Johnson LG, Olsen JC: Influenza M2 envelope protein augments avian influenza hemagglutinin pseudotyping of lentiviral vectors. Gene Ther 2006, 13: 715-724. 10.1038/sj.gt.3302715CrossRefPubMed McKay T, Patel M, Pickles RJ, Johnson LG, Olsen JC: Influenza M2 envelope protein augments avian influenza hemagglutinin pseudotyping of lentiviral vectors. Gene Ther 2006, 13: 715-724. 10.1038/sj.gt.3302715CrossRefPubMed
28.
go back to reference Skehel JJ, Bayley PM, Brown EB, Martin SR, Waterfield MD, White JM, Wilson IA, Wiley DC: Changes in the conformation of influenza virus hemagglutinin at the pH optimum of virus-mediated membrane fusion. Proc Natl Acad Sci U S A 1982, 79: 968-972. 10.1073/pnas.79.4.968PubMedCentralCrossRefPubMed Skehel JJ, Bayley PM, Brown EB, Martin SR, Waterfield MD, White JM, Wilson IA, Wiley DC: Changes in the conformation of influenza virus hemagglutinin at the pH optimum of virus-mediated membrane fusion. Proc Natl Acad Sci U S A 1982, 79: 968-972. 10.1073/pnas.79.4.968PubMedCentralCrossRefPubMed
29.
go back to reference Graves PN, Schulman JL, Young JF, Palese P: Preparation of influenza virus subviral particles lacking the HA1 subunit of hemagglutinin: unmasking of cross-reactive HA2 determinants. Virology 1983, 126: 106-116. 10.1016/0042-6822(83)90465-8CrossRefPubMed Graves PN, Schulman JL, Young JF, Palese P: Preparation of influenza virus subviral particles lacking the HA1 subunit of hemagglutinin: unmasking of cross-reactive HA2 determinants. Virology 1983, 126: 106-116. 10.1016/0042-6822(83)90465-8CrossRefPubMed
30.
go back to reference Sagawa H, Ohshima A, Kato I, Okuno Y, Isegawa Y: The immunological activity of a deletion mutant of influenza virus haemagglutinin lacking the globular region. J Gen Virol 1996, 77 ( Pt 7): 1483-1487.CrossRef Sagawa H, Ohshima A, Kato I, Okuno Y, Isegawa Y: The immunological activity of a deletion mutant of influenza virus haemagglutinin lacking the globular region. J Gen Virol 1996, 77 ( Pt 7): 1483-1487.CrossRef
31.
go back to reference Okuno Y, Isegawa Y, Sasao F, Ueda S: A common neutralizing epitope conserved between the hemagglutinins of influenza A virus H1 and H2 strains. J Virol 1993, 67: 2552-2558.PubMedCentralPubMed Okuno Y, Isegawa Y, Sasao F, Ueda S: A common neutralizing epitope conserved between the hemagglutinins of influenza A virus H1 and H2 strains. J Virol 1993, 67: 2552-2558.PubMedCentralPubMed
32.
go back to reference Yao Q, Kuhlmann FM, Eller R, Compans RW, Chen C: Production and characterization of simian--human immunodeficiency virus-like particles. AIDS Res Hum Retroviruses 2000, 16: 227-236. 10.1089/088922200309322CrossRefPubMed Yao Q, Kuhlmann FM, Eller R, Compans RW, Chen C: Production and characterization of simian--human immunodeficiency virus-like particles. AIDS Res Hum Retroviruses 2000, 16: 227-236. 10.1089/088922200309322CrossRefPubMed
33.
go back to reference Duisit G, Salvetti A, Moullier P, Cosset FL: Functional characterization of adenoviral/retroviral chimeric vectors and their use for efficient screening of retroviral producer cell lines. Human Gene Therapy 1999, 10: 189-200. 10.1089/10430349950018986CrossRefPubMed Duisit G, Salvetti A, Moullier P, Cosset FL: Functional characterization of adenoviral/retroviral chimeric vectors and their use for efficient screening of retroviral producer cell lines. Human Gene Therapy 1999, 10: 189-200. 10.1089/10430349950018986CrossRefPubMed
34.
go back to reference Roberts ML, Wells DJ, Graham IR, Fabb SA, Hill VJ, Duisit G, Yuasa K, Takeda S, Cosset FL, Dickson G: Stable micro-dystrophin gene transfer using an integrating adeno-retroviral hybrid vector ameliorates the dystrophic pathology in mdx mouse muscle. Hum Mol Genet 2003, 11: 1719-1730. 10.1093/hmg/11.15.1719CrossRef Roberts ML, Wells DJ, Graham IR, Fabb SA, Hill VJ, Duisit G, Yuasa K, Takeda S, Cosset FL, Dickson G: Stable micro-dystrophin gene transfer using an integrating adeno-retroviral hybrid vector ameliorates the dystrophic pathology in mdx mouse muscle. Hum Mol Genet 2003, 11: 1719-1730. 10.1093/hmg/11.15.1719CrossRef
35.
go back to reference Savard N, Cosset FL, Epstein AL: Use of defective HSV-1 vectors harbouring gag, pol, and env genes to rescue defective retrovirus vectors. J Virol 1997, 71: 4111-4117.PubMedCentralPubMed Savard N, Cosset FL, Epstein AL: Use of defective HSV-1 vectors harbouring gag, pol, and env genes to rescue defective retrovirus vectors. J Virol 1997, 71: 4111-4117.PubMedCentralPubMed
Metadata
Title
Induction of neutralising antibodies by virus-like particles harbouring surface proteins from highly pathogenic H5N1 and H7N1 influenza viruses
Authors
Judit Szécsi
Bertrand Boson
Per Johnsson
Pia Dupeyrot-Lacas
Mikhail Matrosovich
Hans-Dieter Klenk
David Klatzmann
Viktor Volchkov
François-Loïc Cosset
Publication date
01-12-2006
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2006
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/1743-422X-3-70

Other articles of this Issue 1/2006

Virology Journal 1/2006 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.